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The Gut Microbiota Determines the High-Altitude Adaptability of Tibetan Wild Asses (Equus kiang) in Qinghai-Tibet Plateau

It was acknowledged long ago that microorganisms have played critical roles in animal evolution. Tibetan wild asses (TWA, Equus kiang) are the only wild perissodactyls on the Qinghai-Tibet Plateau (QTP) and the first national protected animals; however, knowledge about the relationships between thei...

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Autores principales: Liu, Hongjin, Han, Xueping, Zhao, Na, Hu, Linyong, Wang, Xungang, Luo, Chongliang, Chen, Yongwei, Zhao, Xinquan, Xu, Shixiao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9342865/
https://www.ncbi.nlm.nih.gov/pubmed/35923394
http://dx.doi.org/10.3389/fmicb.2022.949002
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author Liu, Hongjin
Han, Xueping
Zhao, Na
Hu, Linyong
Wang, Xungang
Luo, Chongliang
Chen, Yongwei
Zhao, Xinquan
Xu, Shixiao
author_facet Liu, Hongjin
Han, Xueping
Zhao, Na
Hu, Linyong
Wang, Xungang
Luo, Chongliang
Chen, Yongwei
Zhao, Xinquan
Xu, Shixiao
author_sort Liu, Hongjin
collection PubMed
description It was acknowledged long ago that microorganisms have played critical roles in animal evolution. Tibetan wild asses (TWA, Equus kiang) are the only wild perissodactyls on the Qinghai-Tibet Plateau (QTP) and the first national protected animals; however, knowledge about the relationships between their gut microbiota and the host's adaptability remains poorly understood. Herein, 16S rRNA and meta-genomic sequencing approaches were employed to investigate the gut microbiota–host associations in TWA and were compared against those of the co-resident livestock of yak (Bos grunnies) and Tibetan sheep (Ovis aries). Results revealed that the gut microbiota of yak and Tibetan sheep underwent convergent evolution. By contrast, the intestinal microflora of TWA diverged in a direction enabling the host to subsist on sparse and low-quality forage. Meanwhile, high microbial diversity (Shannon and Chao1 indices), cellulolytic activity, and abundant indicator species such as Spirochaetes, Bacteroidetes, Prevotella_1, and Treponema_2 supported forage digestion and short-chain fatty acid production in the gut of TWA. Meanwhile, the enterotype identification analysis showed that TWA shifted their enterotype in response to low-quality forage for a better utilization of forage nitrogen and short-chain fatty acid production. Metagenomic analysis revealed that plant biomass degrading microbial consortia, genes, and enzymes like the cellulolytic strains (Prevotella ruminicola, Ruminococcus flavefaciens, Ruminococcus albus, Butyrivibrio fibrisolvens, and Ruminobacter amylophilus), as well as carbohydrate metabolism genes (GH43, GH3, GH31, GH5, and GH10) and enzymes (β-glucosidase, xylanase, and β-xylosidase, etc.) had a significantly higher enrichment in TWA. Our results indicate that gut microbiota can improve the adaptability of TWA through plant biomass degradation and energy maintenance by the functions of gut microbiota in the face of nutritional deficiencies and also provide a strong rationale for understanding the roles of gut microbiota in the adaptation of QTP wildlife when facing harsh feeding environments.
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spelling pubmed-93428652022-08-02 The Gut Microbiota Determines the High-Altitude Adaptability of Tibetan Wild Asses (Equus kiang) in Qinghai-Tibet Plateau Liu, Hongjin Han, Xueping Zhao, Na Hu, Linyong Wang, Xungang Luo, Chongliang Chen, Yongwei Zhao, Xinquan Xu, Shixiao Front Microbiol Microbiology It was acknowledged long ago that microorganisms have played critical roles in animal evolution. Tibetan wild asses (TWA, Equus kiang) are the only wild perissodactyls on the Qinghai-Tibet Plateau (QTP) and the first national protected animals; however, knowledge about the relationships between their gut microbiota and the host's adaptability remains poorly understood. Herein, 16S rRNA and meta-genomic sequencing approaches were employed to investigate the gut microbiota–host associations in TWA and were compared against those of the co-resident livestock of yak (Bos grunnies) and Tibetan sheep (Ovis aries). Results revealed that the gut microbiota of yak and Tibetan sheep underwent convergent evolution. By contrast, the intestinal microflora of TWA diverged in a direction enabling the host to subsist on sparse and low-quality forage. Meanwhile, high microbial diversity (Shannon and Chao1 indices), cellulolytic activity, and abundant indicator species such as Spirochaetes, Bacteroidetes, Prevotella_1, and Treponema_2 supported forage digestion and short-chain fatty acid production in the gut of TWA. Meanwhile, the enterotype identification analysis showed that TWA shifted their enterotype in response to low-quality forage for a better utilization of forage nitrogen and short-chain fatty acid production. Metagenomic analysis revealed that plant biomass degrading microbial consortia, genes, and enzymes like the cellulolytic strains (Prevotella ruminicola, Ruminococcus flavefaciens, Ruminococcus albus, Butyrivibrio fibrisolvens, and Ruminobacter amylophilus), as well as carbohydrate metabolism genes (GH43, GH3, GH31, GH5, and GH10) and enzymes (β-glucosidase, xylanase, and β-xylosidase, etc.) had a significantly higher enrichment in TWA. Our results indicate that gut microbiota can improve the adaptability of TWA through plant biomass degradation and energy maintenance by the functions of gut microbiota in the face of nutritional deficiencies and also provide a strong rationale for understanding the roles of gut microbiota in the adaptation of QTP wildlife when facing harsh feeding environments. Frontiers Media S.A. 2022-07-18 /pmc/articles/PMC9342865/ /pubmed/35923394 http://dx.doi.org/10.3389/fmicb.2022.949002 Text en Copyright © 2022 Liu, Han, Zhao, Hu, Wang, Luo, Chen, Zhao and Xu. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Liu, Hongjin
Han, Xueping
Zhao, Na
Hu, Linyong
Wang, Xungang
Luo, Chongliang
Chen, Yongwei
Zhao, Xinquan
Xu, Shixiao
The Gut Microbiota Determines the High-Altitude Adaptability of Tibetan Wild Asses (Equus kiang) in Qinghai-Tibet Plateau
title The Gut Microbiota Determines the High-Altitude Adaptability of Tibetan Wild Asses (Equus kiang) in Qinghai-Tibet Plateau
title_full The Gut Microbiota Determines the High-Altitude Adaptability of Tibetan Wild Asses (Equus kiang) in Qinghai-Tibet Plateau
title_fullStr The Gut Microbiota Determines the High-Altitude Adaptability of Tibetan Wild Asses (Equus kiang) in Qinghai-Tibet Plateau
title_full_unstemmed The Gut Microbiota Determines the High-Altitude Adaptability of Tibetan Wild Asses (Equus kiang) in Qinghai-Tibet Plateau
title_short The Gut Microbiota Determines the High-Altitude Adaptability of Tibetan Wild Asses (Equus kiang) in Qinghai-Tibet Plateau
title_sort gut microbiota determines the high-altitude adaptability of tibetan wild asses (equus kiang) in qinghai-tibet plateau
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9342865/
https://www.ncbi.nlm.nih.gov/pubmed/35923394
http://dx.doi.org/10.3389/fmicb.2022.949002
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